Sex Differences in the Development of Social Relationships in Rhesus Macaques (Macaca mulatta)

Abstract

Several studies have documented the importance of social bonding for the enhancement of individual fitness. However, little is known about how social relationships develop through ontogeny, and whether their development follows the same trajectory in males and females. Here we analyzed affiliative interactions (proximity, social grooming, play) combined with demographic and genetic data in semi-free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago over their first 4 yr of life (from birth to sexual maturation) to understand how these interactions change through development in both sexes. Generalized linear mixed models revealed that social behaviors mostly followed different developmental trajectories in males and females and were highly dependent on the social context. In particular, sex differences in social behavior varied through development depending on the partner’s sex and age. Females engaged in more social interactions than males, especially with other females, and were more involved in grooming around the time of maturation. In contrast, males interacted more with males and age peers, especially around maturation. Sex differences in social behavior varied through development, but also depended on rank, partner’s rank, and kin line, although not consistently. High-ranking individuals, especially older females, were generally preferred as social partners. Moreover, both male and female individuals interacted mostly with maternal kin, although males also preferred paternal kin over nonkin. Importantly, most developmental changes in sociality happened when individuals were ca. 2 yr old, suggesting that this might be a milestone in the development of sociality in rhesus macaques. The only notable exception to this pattern was play, which was more pronounced in males from the beginning of their lives. We propose that play might serve as a trigger of sex differences in social behavior, with sex differences emerging early in development and increasing through time as males and females gradually grow into their adult social roles.

Sex Differences in the Development of Aggressive Behavior in Rhesus Macaques (Macaca mulatta)

“…However, these results are also consistent with the hypothesis that aggression is directed mostly toward those social partners with which individuals have the strongest affiliative bonds (Bernstein and Ehardt, 1986;Kulik et al 2015;Widdig et al 2002Widdig et al , 2006. In primates, females usually form the strongest social bonds with other females, e.g., rhesus macaques (Kapsalis andBerman 1996), vervets (Cercopithecus aethiops: Seyfarth 1980), capuchins (Cebus capucinus : Perry 1996), and savannah baboons (Seyfarth 1976;Silk et al 1999), and males with males (red colobus, Colobus badius: Struhsaker and Leland, 1976;spider monkeys: Slater et al 2009;muriquis, Brachyteles arachnoids hypoxanthus: Strier et al 2002;chimpanzees: Arnold and Whiten 2003;Gilby and Wrangham 2008;Goodall, 1986;Lonsdorf et al 2014;Nishida 1979;Watts 2000a,b;Wrangham et al 1992).…”

“…Moreover, males share a closer proximity with age peers around maturation, with which they are likely to be closely related owing to high male reproductive skew (Widdig 2013) and are likely to disperse together from their natal group (Albers and Widdig 2013). Finally, males also preferentially direct affiliative behaviors toward females early in development and later on toward males (Kulik et al 2015), further suggesting that the distribution of affiliative and aggressive behaviors partly follows similar patterns. Although in this study we conducted no direct analyses to test the link between affiliative and aggressive behaviors at the dyadic level, it is evident that classes of individuals, e.g., males, maternal kin, and younger individuals, largely share the same preferences when interacting with other classes of individuals both via aggressive and affiliative behaviors (cf.…”

“…Although in this study we conducted no direct analyses to test the link between affiliative and aggressive behaviors at the dyadic level, it is evident that classes of individuals, e.g., males, maternal kin, and younger individuals, largely share the same preferences when interacting with other classes of individuals both via aggressive and affiliative behaviors (cf. Kulik et al 2015). Possibly the distribution of aggressive behavior reflects the association patterns in the social group, with most aggressive interactions taking place between individuals that are often in close proximity and have strong affiliative bonds.…”

“…These results support the suggestion that being aggressive might largely serve a similar function for both sexes during the first years of development, and juvenile aggressive behavior does not necessarily anticipate adult patterns (Cords et al 2010;Eaton et al 1986;Raleigh et al 1979;Wolfheim 1977). Whereas affiliative behavior allows individuals to construct lasting relationships over long time frames (Kulik et al 2015), aggressive behavior might serve more immediate functions, i.e., to solve contingent conflictual situations, and thus fail to completely anticipate future patterns of interactions.…”

“…Aggression can indeed have a positive effect on socialization processes among primates, e.g., by modifying others' inappropriate social behavior (Bernstein andEhardt 1985a, b, 1986) and producing cohesive forces within a social group (Bercovitch et al 1987;Bernstein and Gordon 1974;de Waal 1989). The frequency of aggressive interactions is also often higher in dyads having stronger affiliative relationships (Bernstein and Ehardt 1986;Kulik et al 2015;Widdig et al 2002Widdig et al , 2006cf. Silk et al 1981cf.…”